17
ORIGINAL PAPER Risk management to prioritise the eradication of new and emerging invasive non-native species Olaf Booy . Aileen C. Mill . Helen E. Roy . Alice Hiley . Niall Moore . Pete Robertson . Simon Baker . Matt Brazier . Mathilde Bue . Richard Bullock . Steve Campbell . Dominic Eyre . Jim Foster . Maggie Hatton-Ellis . Jo Long . Craig Macadam . Camilla Morrison-Bell . John Mumford . Jonathan Newman . David Parrott . Robin Payne . Trevor Renals . Eoina Rodgers . Mark Spencer . Paul Stebbing . Mike Sutton-Croft . Kevin J. Walker . Alastair Ward . Stan Whittaker . Gabe Wyn Received: 17 November 2016 / Accepted: 28 April 2017 / Published online: 15 May 2017 Ó The Author(s) 2017. This article is an open access publication Abstract Robust tools are needed to prioritise the management of invasive non-native species (INNS). Risk assessment is commonly used to prioritise INNS, but fails to take into account the feasibility of management. Risk management provides a structured evaluation of management options, but has received little attention to date. We present a risk management scheme to assess the feasibility of eradicating INNS that can be used, in conjunction with existing risk assessment schemes, to support prioritisation. The Non-Native Risk Management scheme (NNRM) can be applied to any predefined area and any taxa. It uses semi-quantitative response and confidence scores to assess seven key criteria: Effectiveness, Practicality, Cost, Impact, Acceptability, Window of opportunity and Likelihood of re-invasion. Scores are elicited using expert judgement, supported by available evi- dence, and consensus-building methods. We applied the NNRM to forty-one INNS that threaten Great Britain (GB). Thirty-three experts provided scores, with overall feasibility of eradication assessed as ‘very high’ (8 species), ‘high’ (6), ‘medium’ (8), ‘low’ (10) Electronic supplementary material The online version of this article (doi:10.1007/s10530-017-1451-z) contains supple- mentary material, which is available to authorized users. O. Booy Á N. Moore Á P. Robertson Á S. Baker Á D. Parrott Á M. Sutton-Croft Á A. Ward National Wildlife Management Centre, Animal and Plant Health Agency, Sand Hutton, York YO41 1LZ, UK O. Booy (&) Á A. C. Mill Á P. Robertson Centre for Wildlife Management, School of Biology, Newcastle University, Newcastle-upon-Tyne NE1 7RU, UK e-mail: [email protected] H. E. Roy Á J. Newman Centre for Ecology and Hydrology, Maclean Building, Benson Lane, Crowmarsh Gifford, Wallingford, Oxfordshire OX10 8BB, UK A. Hiley Á M. Brazier Á T. Renals Environment Agency, Tyneside House, Skinnerburn Road, Newcastle upon Tyne NE4 7AR, UK M. Bue Institute of Biological, Environmental and Rural Sciences, Aberystwyth University, Aberystwyth SY23 3DA, UK R. Bullock Wildfowl and Wetlands Trust, Queen Elizabeth’s Walk, Barnes, London SW13 9WT, UK S. Campbell Science and Advice for Scottish Agriculture, Roddinglaw Road, Edinburgh EH12 9FJ, UK D. Eyre Defra, Sand Hutton, York YO41 1LZ, UK J. Foster Amphibian and Reptile Conservation, The Witley Centre, Witley, Godalming, Surrey GU8 5QA, UK 123 Biol Invasions (2017) 19:2401–2417 DOI 10.1007/s10530-017-1451-z

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Page 1: Risk management to prioritise the eradication of new and

ORIGINAL PAPER

Risk management to prioritise the eradication of newand emerging invasive non-native species

Olaf Booy . Aileen C. Mill . Helen E. Roy . Alice Hiley . Niall Moore .

Pete Robertson . Simon Baker . Matt Brazier . Mathilde Bue . Richard Bullock .

Steve Campbell . Dominic Eyre . Jim Foster . Maggie Hatton-Ellis .

Jo Long . Craig Macadam . Camilla Morrison-Bell . John Mumford .

Jonathan Newman . David Parrott . Robin Payne . Trevor Renals .

Eoina Rodgers . Mark Spencer . Paul Stebbing . Mike Sutton-Croft .

Kevin J. Walker . Alastair Ward . Stan Whittaker . Gabe Wyn

Received: 17 November 2016 / Accepted: 28 April 2017 / Published online: 15 May 2017

� The Author(s) 2017. This article is an open access publication

Abstract Robust tools are needed to prioritise the

management of invasive non-native species (INNS).

Risk assessment is commonly used to prioritise INNS,

but fails to take into account the feasibility of

management. Risk management provides a structured

evaluation of management options, but has received

little attention to date. We present a risk management

scheme to assess the feasibility of eradicating INNS

that can be used, in conjunction with existing risk

assessment schemes, to support prioritisation. The

Non-Native Risk Management scheme (NNRM) can

be applied to any predefined area and any taxa. It uses

semi-quantitative response and confidence scores to

assess seven key criteria: Effectiveness, Practicality,

Cost, Impact, Acceptability, Window of opportunity

and Likelihood of re-invasion. Scores are elicited

using expert judgement, supported by available evi-

dence, and consensus-building methods. We applied

the NNRM to forty-one INNS that threaten Great

Britain (GB). Thirty-three experts provided scores,

with overall feasibility of eradication assessed as ‘very

high’ (8 species), ‘high’ (6), ‘medium’ (8), ‘low’ (10)Electronic supplementary material The online version ofthis article (doi:10.1007/s10530-017-1451-z) contains supple-mentary material, which is available to authorized users.

O. Booy � N. Moore � P. Robertson � S. Baker �D. Parrott � M. Sutton-Croft � A. Ward

National Wildlife Management Centre, Animal and Plant

Health Agency, Sand Hutton, York YO41 1LZ, UK

O. Booy (&) � A. C. Mill � P. RobertsonCentre for Wildlife Management, School of Biology,

Newcastle University, Newcastle-upon-Tyne NE1 7RU,

UK

e-mail: [email protected]

H. E. Roy � J. Newman

Centre for Ecology and Hydrology, Maclean Building,

Benson Lane, Crowmarsh Gifford, Wallingford,

Oxfordshire OX10 8BB, UK

A. Hiley � M. Brazier � T. RenalsEnvironment Agency, Tyneside House, Skinnerburn

Road, Newcastle upon Tyne NE4 7AR, UK

M. Bue

Institute of Biological, Environmental and Rural Sciences,

Aberystwyth University, Aberystwyth SY23 3DA, UK

R. Bullock

Wildfowl and Wetlands Trust, Queen Elizabeth’s Walk,

Barnes, London SW13 9WT, UK

S. Campbell

Science and Advice for Scottish Agriculture, Roddinglaw

Road, Edinburgh EH12 9FJ, UK

D. Eyre

Defra, Sand Hutton, York YO41 1LZ, UK

J. Foster

Amphibian and Reptile Conservation, The Witley Centre,

Witley, Godalming, Surrey GU8 5QA, UK

123

Biol Invasions (2017) 19:2401–2417

DOI 10.1007/s10530-017-1451-z

Page 2: Risk management to prioritise the eradication of new and

and ‘very low’ (9). The feasibility of eradicating

terrestrial species was higher than aquatic species.

Lotic freshwater and marine species scored particu-

larly low. Combining risk management and existing

risk assessment scores identified six established

species as priorities for eradication. A further six

species that are not yet established were identified as

priorities for eradication on arrival as part of contin-

gency planning. The NNRM is one of the first INNS

risk management schemes that can be used with

existing risk assessments to prioritise INNS eradica-

tion in any area.

Keywords Risk analysis � Resource management �Feasibility of eradication � Contingency planning �Great Britain � NNRM

Introduction

Decision-makers are under growing pressure to

respond to invasive non-native species (INNS)

(Hulme 2006; Seebens et al. 2017) and require

transparent evidence on which to base decisions

(Sutherland et al. 2004). Given the large and increas-

ing numbers of species involved (Pimentel et al. 2005;

Daisie 2009; Hulme 2009; Roy et al. 2014a), the often

high costs associated with management and limited

resources, there is a need for management to be

carefully prioritised (McGeoch et al. 2016; Early et al.

2016). However, practical, transparent and robust

tools to support the prioritisation of management are

lacking (Hulme et al. 2009).

One way of prioritising INNSmanagement is to use

risk analysis, which traditionally includes hazard

identification, risk assessment, risk management and

risk communication (Vanderhoeven et al. 2017). It is

the balance between risk assessment and risk man-

agement that allows for prioritisation, with risk

assessment used to assess the threat or hazard of a

species and risk management used to evaluate and

implement management options (FAO 1995). Within

this framework, high risk species for which manage-

ment is cost effective are prioritised first and low risk

species for which management is expensive and

ineffective are prioritised last. Both risk assessment

and risk management are essential for prioritisation;

however, while numerous INNS risk assessment

schemes have been developed (for reviews see Early

et al. 2016; Heikkila 2011; Leung et al. 2012; Roy

et al. 2014b; Verbrugge et al. 2010) very few exist for

risk management (Heikkila 2011; Vanderhoeven et al.

2017). Of the schemes that do include elements of risk

management, many only include one or few questions

(e.g. Essl et al. 2011; Vanderhoeven et al. 2015) or

provide an evaluation of what is advisable, but not an

indication of priority (Schmiedel et al. 2016). While

more elaborate schemes are available for weed risk

management and plant health pests, these are limited

M. Hatton-Ellis � G. Wyn

Natural Resources Wales, Maes y Ffynnon, Penrhos Rd,

Bangor LL572DW, UK

C. Morrison-Bell

British Ecological Society, Charles Darwin House, 12

Roger Street, London WC1N 2JU, UK

J. Long

Scottish Environment Protection Agency, Strathallan

House, Castle Business Park, Stirling FK9 4TZ, UK

C. Macadam

Buglife, Balallan House, 24 Allan Park,

Stirling FK8 2QG, UK

J. Mumford

Imperial College London, Silwood Park Campus, Ascot,

Berkshire SL5 7PY, UK

R. Payne

Airlie Bank, Bamff Road, Alyth PH11 8DR, Scotland, UK

E. Rodgers

Royal Society for the Prevention of Cruelty to Animals,

Wilberforce Way, Southwater RH13 9RS, UK

M. Spencer

Natural History Museum, Cromwell Road,

London SW7 5BD, UK

P. Stebbing

Centre for Environment, Fisheries and Aquaculture

Science, The Nothe, Barrack Road, Weymouth,

Dorset DT4 8UB, UK

K. J. Walker

Botanical Society of Britain and Ireland, Natural History

Museum, Cromwell Road, London SW7 5BD, UK

S. Whittaker

Scottish Natural Heritage, Silvan House, Corstorphine

Road, Edinburgh EH12 7AT, UK

2402 O. Booy et al.

123

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by being taxonomically or sector specific (e.g. Auld

2012; Baker et al. 2005; Drolet et al. 2014; Firn et al.

2015a, b; Hiebert and Stubbendieck 1993; Kehlenbeck

et al. 2012; Setterfield et al. 2010; Sunley et al. 2012;

Virtue 2010), consider only specific aspects of risk

management (e.g. Darin 2008; Hauser and McCarthy

2009; Darin et al. 2011; Liu et al. 2011) or being time

and resource intensive (e.g. Darin et al. 2011; Leung

et al. 2012; McGeoch et al. 2016; Vander Zanden et al.

2010).

There is, therefore, a need for a practical risk

management scheme that is compatible with existing

risk assessment schemes in order to support prioriti-

sation of INNS (D’hondt et al. 2015). Given the range

of species that become invasive, such a scheme should

be broadly applicable to any taxa (Nentwig et al. 2010)

and, given large numbers of species involved, should

be efficient to apply (Andersen et al. 2004; Hulme

et al. 2009). It should be possible to complete the

scheme even where data are lacking, with uncertainty

taken into account, documented and justified (Leung

et al. 2012; Vanderhoeven et al. 2017).

We set out to develop a scheme, known as the Non-

Native Risk Management Scheme (NNRM), that

meets these criteria and complies with international

standards for risk management (FAO 1995, 2006; OIE

2015) as well as good practice for prioritisation

(summarised by Heikkila 2011). We focussed on

assessing the feasibility of eradication (sensu Gen-

ovesi 2000), acknowledging that eradication is the

most effective management response after prevention

(Genovesi 2005). It is also the focus of the second tier

in the hierarchical approach to INNS management

(Guiding Principle 2, COP 6 decision VI/23, Conven-

tion on Biological Diversity) as well as an important

component of Aichi Target 9 (UNEP 2011). To ensure

it could be practically applied and completed even

where data were limited, the NNRM was designed to

use expert judgement (Martin et al. 2012) to provide

semi-quantitative scores (sensu Baker et al. 2008)

which are justified by written comments, and sup-

ported by evidence where available. This follows

similar approaches used for risk assessment (Baker

et al. 2008, 2012; Essl et al. 2011; Leung et al. 2012).

To demonstrate its use we trialled the scheme in

GB, which has a well-developed and robust INNS risk

assessment process but lacks a compatible process for

risk management (Defra 2015). We applied the

scheme to a group of new and emerging INNS that

pose a threat to GB, as these were considered most

likely to be potential candidates for eradication (Roy

et al. 2014c). We demonstrate how the scheme can be

used, in combination with existing risk assessment

scores, to indicate priorities for eradication and

contingency planning; and examine the importance

of risk management for prioritisation. While applied

here to GB, the scheme can be applied at different

scales and in different areas worldwide. Indeed, the

scheme may have particular application in the EU

where the recent adoption of Regulation No.

1143/2014 includes requirements for eradication of

INNS listed on the basis of both risk assessment and

risk management variables (EU 2014).

Materials and methods

Development

The Non-Native Risk Management Scheme (NNRM)

was developed over a 2-year period from 2013 to 2015

in collaboration with INNS management and risk

analysis experts from Great Britain (GB). Initial

criteria were developed in consultation with this group

taking into consideration existing literature on INNS

risk analysis and eradication (in particular Baker et al.

2005; Cacho et al. 2006; Cunningham et al. 2003;

Genovesi 2005, 2007; Hiebert and Stubbendieck

1993; Hulme 2006; Johnson 2009; Kehlenbeck et al.

2012; Mehta et al. 2010; Randall et al. 2008;

Rejmanek and Pitcairn 2002; Simberloff 2003, 2009;

Sunley et al. 2012; Virtue 2010). Refinements were

made to the scheme during an initial trial in March

2014 and subsequently the expert elicitation and

consensus-building process described below. Deci-

sion-makers were engaged in the initial development

of the scheme and at intervals throughout the process

to ensure the relevance of the scheme for them as end-

users.

The non-native risk management scheme

The NNRM takes the form of a questionnaire

supported by guidance (S1), which is summarised in

Box 1. Preliminary stages record the details of

authors, the organism to be assessed, the risk man-

agement area and the objective of the assessment. The

risk management area is user defined to allow any area

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to be assessed, but must be precisely defined. The

objective of the assessment is set from the outset as the

complete eradication of the organism from the risk

management area (sensu Genovesi 2000).

Once preliminary stages are complete, the assess-

ment is started by documenting the invasion scenario

(Box 1, step 1), which describes the extent of the

INNS in the risk management area (see guidance in S1

for detail). The scenario may be based on known

existing or predicted future invasions, as well as

probabilistic scenarios such as best, most likely, or

worst case scenarios; however, for assessments to be

comparable the scenario selected must be consistent

(to this end the most likely scenario was adopted for all

assessments in the trial described below). Multiple

scenarios may be considered for individual species, in

which case each scenario is assessed separately. In all

cases assessors should carefully document the sce-

nario being considered, along with any assumptions

made, to provide context for the results.

The eradication strategy is then defined (Box 1,

step 2). This is a realistic strategy considered likely to

achieve complete eradication of the species from the

defined risk management area and can include any

combination of individual methods (e.g. use of

pesticides, herbicides, trapping, shooting, etc.). Mul-

tiple eradication strategies can be considered if

necessary to allow for comparison between different

approaches, in which case each strategy should be

separately assessed. Assessors determine which strat-

egy they consider likely to achieve eradication,

avoiding being too conservative (i.e. no eradication

possible despite techniques being available) or unre-

alistic (i.e. cost/damage caused vastly outweighs

potential benefits). If no realistic eradication strategy

can be determined then the species automatically

scores very low overall feasibility of eradication and

comments are provided to justify this decision. As

with the invasion scenario, defining the eradication

strategy at this point allows for assumptions to be

Box 1 Summary of guidance provided to complete risk management assessments; the full scheme is available (S1)

1. Define the invasion scenario. For species that are already established this is the current extent of the species in the risk

management area. For species on the horizon this is the most likely extent of the species in the risk management area at the point

detection could reasonably be expected (based on existing surveillance)

2. Define the eradication strategy. Based on the defined scenario briefly describe the eradication strategy being assessed. This

should be a realistic strategy you consider most likely to be effective in eradicating the species completely from the risk

management area. The overall strategy could include multiple methods (e.g. use of pesticides, herbicides, trapping, shooting,

etc.) and should include any other work that would be required such as surveys, logistics and monitoring

3. Assess the eradication strategy:

(a) Effectiveness. How effective would the eradication strategy be? This relates to how effective the defined strategy would be if

it could be deployed regardless of issues with practicality, cost, impact and acceptability

(b) Practicality. How practical would it be to deliver the eradication strategy? This includes issues such as gaining access to

relevant areas, obtaining appropriate equipment, skilled staff or pesticides. If there are any legal barriers to undertaking the work

these are assessed here

(c) Cost. How much would the eradication strategy cost? This is the total direct cost of the strategy including materials, staff

time and any other direct costs. Indirect costs, such as loss of business, are taken into account under negative impact (3d)

(d) Negative impact. What negative impact would the eradication strategy have? Assess the impact that the eradication strategy

itself would have on the environment, economy or society

(e) Acceptability. How acceptable is the eradication strategy? Could the eradication strategy meet significant disapproval or

resistance from the general public, key sectors or any other stakeholder?

4. Assess the window of opportunity for delivering the described eradication strategy. How quickly will the species spread beyond

the point that eradication, using the defined strategy, would be effective?

5. Assess the likelihood of re-invasion following eradication. Unless the eradication strategy deliberately targets populations in

containment or otherwise not in the wild (i.e. in gardens, zoos, etc.) introduction from these sources should be considered

potential sources of re-invasion. If relevant, the eradication strategy could include pathway management measures in order to

reduce this score

6. Overall feasibility of eradication. Taking into account all preceding scores, provide an overall score for the feasibility of

eradicating this species from the risk management area

The risk management objective was set as complete eradication from GB for all species

2404 O. Booy et al.

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documented and a clear basis for the rest of the

assessment to be set.

The feasibility of eradication, based on the defined

eradication strategy, is then assessed using seven key

questions relating to Effectiveness, Practicality, Cost,

Impact, Acceptability, Window of opportunity and

Likelihood of reinvasion (Box 1, steps 3a–e, 4 and 5).

Lastly, the assessor provides a single overall score for

the feasibility of eradication (Box 1, step 6), which is

based on their expert judgement taking account of the

scenario and responses made in the previous steps.

The overall score is not directly calculated from

individual scores, because no appropriate weighting

could be identified that would account for the wide

range of taxa and criteria being assessed (Mumford

et al. 2010). Instead we used expert judgement based

on previous steps, which follows the approach used

by the UK, EPPO and other risk assessment schemes

(Baker et al. 2012; Mumford et al. 2010) and

provides flexibility, while ensuring overall scores

are supported by individual scores and documented

justification.

Response and confidence scores

For each of the seven questions and the overall

conclusion a response and confidence score are

required with justification provided by a written

comment. Response scores are ordinal on a five-point

scale with one being least favourable and five being

most (Table 1). Each alternative response is prede-

fined using descriptive terms (similar to those used in

risk assessment schemes, e.g. Baker et al. 2008, 2012),

except for Cost and Window of opportunity which is

based on quantified bands. Bands for Cost scores were

determined in consultation with decision makers that

hold national budgets for INNS control and reflect the

range of costs associated with historical eradication

attempts that have been made in GB (if applied to

other countries/regions these bands may need to be

recalibrated). Window of opportunity was quantified

in consultation with risk management experts to reflect

timescales likely to be relevant to a wide range of taxa.

Confidence scores are explicitly recorded for every

response using a three point scale (low, medium high)

following Mumford et al. (2010), which in turn is

based on a simplification of guidance provided by the

Intergovernmental Panel on Climate Change (Mas-

trandrea et al. 2011).

Applying the scheme to new and emerging threats

to GB

The scheme was used to assess 41 new or emerging

INNS that pose a threat to GB and represent a broad

range of taxa and environments (Tables 2, 3a, b).

Twenty species were already established in GB at the

time of assessment, but with limited distributions; a

further 21 were horizon species, defined as species not

established in GB at the time of assessment but

considered likely to invade in the near future. The list

of horizon species was based on the top 30 threats

identified by Roy et al. (2014c), less nine species that

were excluded. Species were excluded if they were

primarily crop, forestry or fish pests and dealt with by

established plant or fish health regimes in GB; or were

species that had already established in GB by the time

of assessment, in which case they were included as

established species. The remaining established species

were selected based on their limited distributions in

GB and because they were being considered for

potential eradication by national policy makers in GB.

The most likely scenario was used for all species,

which for established species was defined as the

species’ current extent, and for horizon species was the

most likely extent at the point of detection with

existing surveillance.

We used expert judgement (supported by evidence

where available) to elicit scores, which is practical but

must be used carefully to minimise the impacts of

subjectivity, bias and group think (Burgman et al.

2011; Martin et al. 2012; Sutherland and Burgman

2015). To this end we followed the approach used by

Roy et al. (2014c) which combines expert elicitation

with review and consensus building to reduce these

effects, while still being practical and efficient to

apply. Techniques incorporated within this approach

include: (a) the structured use of groups rather than

individuals to produce scores, (b) independent initial

scoring followed by review and consensus building;

(c) transparent, documented justification of all scores;

(d) initial presentations and discussion around the

scoring method and terminology to reduce the poten-

tial for language based misunderstanding; (e) open

facilitator-led discussions to encourage all participants

to listen to one another, asses each other’s judgements

and cross examine reasoning behind scores; (f) break-

out sessions to provide smaller and more informal

space in which to express views; and (g) agreeing final

The eradication of new and emerging invasive non-native species 2405

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scores through a facilitator-led discussion where every

participant was directly invited to comment on each

score. We did not attempt to weight individual expert

judgements because of practical problems associated

with constructing reliable and valid weights (Bolger

and Rowe 2015).

In total, 33 experts were engaged in the elicitation

process divided into four groups comprising 7–10

experts each: freshwater animals; terrestrial animals;

marine species; and plants, excluding marine plants.

Experts were selected based on their proven experi-

ence of INNS management in GB and diversity of

background (i.e. government, non-government, prac-

titioners, academics and policy advisors). Experts

were provided with guidance (S1) and instructions to

carry out their assessments. They were encouraged to

discuss any points of clarification either with their

group leader or the organisers. Clarification of any

points was circulated to all experts for consistency.

Initial risk management assessments were drafted over

a period of 7 weeks by experts from each group using

published or grey literature to support scores and

expert judgement where other forms of evidence were

lacking or inconclusive. The task of completing

assessments was shared between experts, with each

species being assessed by a single expert. Drafted

assessments were then circulated to other experts in

the group to provide an initial opportunity for review

and comment before the consensus building

workshop.

The consensus building workshop took place on 28

April 2015 and attended by 19 of the original experts

(limited due to availability), with the drafted risk

management assessments used as the basis of the

Table 1 Assessment criteria for response scores, 1 is least favourable and 5 the most

Criteria Response score

1 2 3 4 5

Effectiveness Very ineffective Ineffective Moderate

effectiveness

Effective Very effective

Practicality Very impractical Impractical Moderate

practicality

Practical Very practical

Cost [£10 M £1–10 M £200 k–1 M £50–200 k \£50 k

Negative impact Massive Major Moderate Minor Minimal

Acceptability Very

unacceptable

Unacceptable Moderate

acceptability

Acceptable Very

acceptable

Window of opportunity \2 months 2 months–

1 year

1–3 years 4–10 years [10 years

Likelihood of reinvasion Very likely Likely Moderate likelihood Unlikely Very unlikely

Conclusion (overall feasibility of

eradication)

Very low Low Medium High Very high

Table 2 Establishment status and environment of species used to test the risk management scheme

Taxa Environment Status in GB

Terrestrial Freshwater Marine Established Not established

Plants 5 5 1 8 3

Vertebrates 10 3 0 6 7

Invertebrates 2 8 7 8 9

Totals 17 16 8 22 19

Species were selected using the list of the top 30 horizon scanning species for Great Britain (Roy et al. 2014c) as well as species with

limited distribution currently being considered for eradication by national policy makers in GB

2406 O. Booy et al.

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Table 3 Risk management scores

The eradication of new and emerging invasive non-native species 2407

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Table 3 continued

2408 O. Booy et al.

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workshop. The first phase of the workshop com-

menced in plenary with a presentation and discussion

around the criteria and scoring approach, followed by

presentations of initial scores by group leaders with all

workshop participants invited to discuss scores and

provide challenge. The aim of this exercise was to

provide an opportunity to resolve any ambiguity about

the process, encourage consistency in scoring between

expert groups and review scores. After initial scores

had been considered by all participants the expert

groups were reformed to discuss and agree alteration

of scores if necessary.

In the second phase of the workshop the facilitators

presented the refined scores for all species in plenary

to all participants. Participants were asked to review

and modify these scores if necessary. By the end of

this second phase, all response and confidence scores

were agreed by the consensus of all participants.

Analysis

We examined individual relationships between overall

score and the sub-scores for the seven detailed risk

management questions using polychoric correlations

as the scores were ordinal from 1 to 5 (see Table 1).

We carried out a factor analysis of the individual

scores and examined the relationship between scores

for all 41 species using non–metric multi-dimensional

scaling (nMDS). Changes to all confidence scores (i.e.

for each of the seven risk management questions and

the overall score) were assessed from the initial scores

to final scores at the end of the second phase of the

workshop.

To indicate priorities for eradication a matrix was

used to compare overall risk management scores with

existing risk assessment scores (Fig. 3). Within this

matrix, species that scored the highest risk and highest

Table 3 continued

Species are grouped according to the overall feasibility of eradication from Great Britain. Colours and numbers reflect response

scores (see Table 1) with overall feasibility of eradication scored from 1 (very low) to 5 (very high). Confidence, rated L (low), M

(medium) and H (high), was recorded for all response scores, but for simplicity is only provided here for overall score. Broad

taxonomic group (Invert. invertebrate, Amp. amphibian, Rept. reptile, Mam. mammal) is provided as well as main environment in

which the species occurs (M marine, F freshwater, T terrestrial)

The eradication of new and emerging invasive non-native species 2409

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feasibility of eradication were given greatest priority,

while species that scored less on either axis were lower

priority. A symmetric relationship between risk assess-

ment and risk management scores was assumed, such

that a species of ‘high’ risk and ‘medium’ feasibility of

eradication received the same priority as a species of

‘medium’ risk and ‘high’ feasibility of eradication. Risk

assessment scores were derived from published data,

with the GB Non-native Risk Assessment

scheme (Baker et al. 2008) providing data for estab-

lished species (published at www.nonnativespecies.

org) and Roy et al. (2014c) providing data for horizon

species. These two schemes differ in that the GB Non-

native Risk Assessment scheme provides an overall

score of high, medium or low risk; whereas horizon

species were all assessed as high risk by Roy et al.

(2014c) and were then further sub-divided into the top

10, top 20 and top 30 threats. This difference is reflected

in the two prioritisation matrices produced.

Results

Risk management scores for all 41 established and

horizon species were agreed by consensus (Table 3a,

b). There was a broad spread of scores for overall

feasibility of eradication, with 13–25% of the species

falling into each of the five possible response

categories (i.e. 1—very low to 5—very high).

The score for overall feasibility of eradication was

most strongly correlated with the risk management

components Practicality (polychoric correlation ±

standard error 0.97 ± 0.02), Effectiveness (0.93 ± 0.03)

and to a lesser extent Cost (0.64 ± 0.1). There was no

significant correlation between overall feasibility of

eradication and Impact, Acceptability, Window of oppor-

tunity or Likelihood of reinvasion (Fig. 1a).

The data were too sparse to predict overall feasi-

bility of eradication by modelling sub-scores (i.e.

scores from each of the seven key risk management

questions). However, accounting for inter-correlations

through a factor analysis and nMDS showed the

overall assessment of feasibility of eradication broadly

relates to the underlying sub-scores (Fig. 1b). Coor-

dinate one of the nMDS correlated with overall

feasibility of eradication, with minimal overlap of

overall scores except between scores 1 and 2 (i.e. ‘very

low’ overall feasibility and ‘low’ feasibility of erad-

ication respectively).

Both response and confidence scores were refined

during the workshop, with 26% of response scores and

58% of confidence scores modified during the first

phase, and 5% of response and 2% of confidence

scores further modified during the second phase.

Confidence increased from the initial scores (propor-

tion of all confidence scores: low = 13%, med-

ium = 87%, high = 0%) to the final scores at the

end of the second phase (proportion of all confidence

scores: low = 8%, medium = 39%, high = 52%). A

similar number of response scores increased as

decreased. Changes in the response and confidence

scores for the seven key risk management questions

tended to result in similar changes to the scores for

overall feasibility of eradication.

We found differences in scores for overall feasibil-

ity of eradication between environments (v2 = 23.73,

df = 8, p =\0.01), with terrestrial species generally

scoring ‘very high’, ‘high’ or ‘medium’ feasibility;

freshwater species scoring ‘medium’ or lower feasi-

bility; and marine species scoring ‘low’ or ‘very low’

feasibility (Fig. 2). We did not detect differences

between taxonomic groups, although the representa-

tive sample size for each group was low.

The scores for overall feasibility of eradication

were combined with overall risk assessment scores to

produce separate prioritisation matrices for estab-

lished and horizon species (Fig. 3a, b). Overall, 12 of

the 41 species assessed scored ‘high’, ‘very high’ or

‘highest’ priority for eradication. Established species

were divided into four groups of differing priority

ranging from ‘very high’ to ‘low’ priority with each

group comprising 2–8 species and six species scoring

‘high’ or ‘very high’ priority. Horizon species were

divided into seven groups of differing priority ranging

from ‘highest’ to ‘lowest’ with each group comprising

1–5 species and six species scoring ‘high’, ‘very high’

or ‘highest’ priority. There was no positive correlation

demonstrated between risk assessment and risk man-

agement (Fig. 3a, b) and the combination of the two

provided information not apparent when considering

either risk assessment or risk management in isolation.

Discussion

We demonstrate that the NNRM is a practical

scheme that can be used to assess a wide range of

taxa from different environments and directly

2410 O. Booy et al.

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compare them according to the overall feasibility of

eradication. It complies with international standards

for risk management (FAO 1995; OIE 2015) and good

practice for non-native species prioritisation (sum-

marised by Heikkila 2011) and is compatible with

existing risk assessment schemes (Baker et al.

2008, 2012). In conjunction with risk assessment

scores, the NNRM can be used to indicate priorities for

eradication of existing and future invasive non-native

species. With increasing legislative requirements to

manage INNS, decision makers require a rapidly

applied, transparent and defendable process by which

Fig. 1 Factor analysis and

non-metric multi-

dimensional scaling

(nMDS) showing

relationship between overall

feasibility of eradication and

subscores (i.e.

Effectiveness, Practicality,

Cost, Impact, Acceptability,

Window of opportunity and

Likelihood of reinvasion).

a Factor analysis showing

correlation between risk

management sub-scores.

The contribution of each

factor to each dimension is

represented by the length

and colour of arrows and

overall explain 72.2% of the

variance in the data. Parallel

arrows indicate correlation

of factors. b Non-metric

multi-dimensional scaling

of sub-scores with each

species coloured by overall

feasibility of eradication

score. The shaded ellipses

are a visual aid centred

around the mean showing

variation (scaled shape and

size of the ellipse) of overall

score. Coordinate 1

correlated well with overall

feasibility of eradication

(1–5)

The eradication of new and emerging invasive non-native species 2411

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eradication actions can be prioritised for established

species, and contingency plans developed for horizon

species (Early et al. 2016). Not only does the NNRM

facilitate risk based policy making in relation to the

eradication of INNS, but also indicates other potential

management actions where feasibility of eradication is

low (e.g. targeted measures to prevent introduction or

containment measures) as well as providing broad

estimates of cost allowing for more effective budget

management. While applied here to GB, the

scheme can be applied to any defined area.

We found that expert scoring, based on predefined

semi-quantitative scales, coupled with consensus

building methods, was a practical way of eliciting

robust standardised risk management scores across

taxa and environment, even where data were incom-

plete or uncertain. It was important to reduce the

potential impact of subjectivity and bias, which we did

following the approach of Roy et al. (2014c). This also

provided additional benefits in the exchange of

knowledge between a diverse group of experts that

do not regularly engage, leading to the challenge of

preconceptions about management in some cases.

While we found this approach was effective and

practical, good practice in the use of experts continues

to develop and should be considered in further

applications of the scheme. This could include

providing additional training steps for scorers using

known data, using and evaluating scoring intervals and

using multiple experts to independently score species

before and after discussions (Hanea et al. 2016; Martin

et al. 2012; Sutherland and Burgman 2015).

A key aim of the consensus workshop was to

provide an opportunity to refine scores based on

knowledge exchange between experienced INNS

managers and to ensure participants had a clear and

consistent understanding of the guidance. This

resulted in a number of changes to scores throughout

the workshop, the majority of which were made during

the first phase, which was the first opportunity

participants had to make refinements following clar-

ification of the guidance and extensive discussions

within and between expert groups. The decrease in the

number of changes made to assessment scores

between the first and second phase of the workshop

demonstrates consensus amongst the experts being

achieved. Confidence scores increased throughout the

workshop with the majority of scores increasing by

one degree (i.e. from medium to high) during the first

phase. While expert judgement often suffers from

overconfidence (Hulme 2012; Morgan 2014), this

suggests that individual assessors were initially cau-

tious when providing draft scores, but confidence

improved with clarification of the guidance and the

benefit of collective experience. The increase in

confidence was a consistent pattern across all expert

groups, suggesting it was not driven by one or two

individuals convincing others.

The strong correlation between overall score and

Practicality, Effectiveness and to a lesser degree Cost

indicates that these components are the most consis-

tent factors when considering overall feasibility of

eradication. The lack of correlation with Likelihood of

reinvasion and Window of opportunity indicates that

these components carry less weight in determining the

overall feasibility of eradication; however, they do

provide important additional information that may

influence resource allocation and the timing of man-

agement. For example, while the purple pitcher-plant

(Sarracenia purpuria) received a high score for

overall feasibility of eradication, it received only a

medium score for Likelihood of reinvasion, suggest-

ing that if eradication were attempted, effort would be

required to prevent reinvasion through further delib-

erate planting in the wild by carnivorous plant

enthusiasts. Impact and Acceptability also did not

correlate strongly with overall score, but did have a

pronounced impact on the overall feasibility of

eradication for some species. For example, while

Carolina fanwort (Cabomba caroliniana) occurs in

only one location in GB, the feasibility of its

Fig. 2 Overall feasibility of eradicating species based on

environment: T terrestrial, F freshwater, M marine. Overall

feasibility of eradication is shown as a proportion of the species

assessed

2412 O. Booy et al.

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eradication was substantially reduced by high levels of

impact and low levels of acceptability associated with

repeated mechanical control (and potential dredging)

where it occurs in an ecologically sensitive Site of

Special Scientific Interest.

We looked for systematic differences in feasibility

of eradication across species to explain potential

drivers that could further inform prioritisation or

management. There was a strong relationship between

overall feasibility of eradication and environment,

Fig. 3 Using overall risk management and risk assessment

scores to indicate priorities for eradication of a established

species and b horizon species. The background colour of the

matrix indicates priority (from green = lowest, to

black = highest). Initials indicate the position of each species

with coloured box representing environment (purple = marine,

blue = freshwater, green = terrestrial). Where multiple spe-

cies occur in one cell they have equal priority and are in no

particular order. The accompaning tables show species lists in

priority order. a Prioritisation matrix for eradicating species

already established in GB. Risk assessment scores derived from

published risk assessments (available at www.nonnativespecies.

org). b Prioritisation matrix for eradication of horizon species

based on most likely scenario of invasion in GB. All horizon

species were scored as high risk and further grouped into the top

10, top 20 and top 30 threats (i.e. upper 10/30; mid 10/30; and

lower 10/30) (Roy et al. 2014c)

The eradication of new and emerging invasive non-native species 2413

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with terrestrial species receiving significantly higher

scores than aquatics, which broadly reflects the

findings of Genovesi (2005), Robertson et al. (2016)

and Simberloff (2009). Freshwater species generally

received low scores; however, eradication was more

likely to be feasible if the species occurred in lentic

(still) rather than lotic (flowing) systems. Eradication

of marine INNS is notably difficult (Sambrook et al.

2014; Thresher and Kuris 2004) and this group

received lowest scores overall. However, eradication

in the marine environment may still be feasible when

specific conditions are met (e.g. Bax et al. 2002;

Culver and Kuris 2000; Wotton et al. 2004), and this is

reflected in the result for Japanese sting winkle

(Ocenebra inornata). We found no correlation

between taxa and overall feasibility of eradication in

our data; however, terrestrial vertebrates generally

received moderate or higher scores for feasibility of

eradication, which reflects experience from GB and

elsewhere (Genovesi 2005; Robertson et al. 2016).

When combined with existing risk assessment

scores our results demonstrate that the NNRM

scheme can be used to prioritise the eradication of

large numbers of non-native species across different

taxa and environment. We identified 12 out of 41

species that pose a threat to GB as ‘high’, ‘very high’

or ‘highest’ priority for eradication. These priorities

are different from those that would result from either

risk assessment or risk management alone, indicating

that taking both into account provides a more refined

approach to prioritisation.

Both established and horizon species can be

assessed using the NNRM scheme, allowing for

emerging species to be prioritised for eradication and

contingency planning to be put in place for new

species before they arrive. Six out of the 20 species

established in GBwere identified as ‘high’, ‘very high’

or ‘highest’ priority for eradication. For these, the

extent of establishment appears to be an important

factor in determining priorities in some cases (four of

the six occurred in one or few small, isolated

populations); however, it was not a reliable predictor

of priority (three of the seven ‘low priority’ species

were established in two or fewer populations, while

two ‘high priority’ species were comparatively wide-

spread). Of the horizon species, six out of 21 were

prioritised as ‘high’, ‘very high’ or ‘highest’ priority

for eradication in GB. Prioritising the eradication of

these species in advance of an invasion allows for

contingency plans to be developed that may increase

the efficiency and effectiveness of a response, which is

particularly important for species that have a short

window of opportunity for eradication, such as the

Asian hornet (Vespa velutina). Indeed, such plans are

already in place in GB for three of the six priority

horizon species identified (published at www.

nonnativespecies.org).

Species that are not considered a high priority for

eradication may be high priorities for other types of

management action. For example, prevention is likely

to be a particularly important for high risk species that

are not yet established in GB and for which eradication

on arrival is unlikely to be feasible. Our results

indicate this is likely to be the case for most marine

and many freshwater (particularly lotic) INNS, in

particular broadleaf watermilfoil (Myriophyllym

heterophylum), American lobster (Homarus ameri-

canus) and round goby (Neogobius melanostomus).

For established species, long term management (e.g.

containment or control) may be a priority for those that

score high risk and low feasibility of eradication, such

as quagga mussel (Dreissena bugensis).

Care should be taken when considering the results

of this work in the context of past eradications in GB,

as the latter were not the result of a systematic and

comprehensive prioritisation process but rather an ad

hoc approach largely driven by particular stakeholders

or specific political drivers (Sheail 2003). However,

some parallels can be drawn as well as exceptions

highlighted. Our results indicate that terrestrial and

lentic freshwater species are more likely to be

priorities for eradication than marine or lotic fresh-

water species, and this already has been the case in GB

where eradications, either complete or underway, have

been instigated for terrestrial vertebrates (Himalayan

porcupine, Hystrix brachyuran; coypu, Myocastor

coypus; muskrat, Ondatra zibethicus (Baker 2010);

monk parakeet, Myiopsitta monachus; ruddy duck,

Oxyura jamaicensis (Defra 2015; Robertson et al.

2015) and lentic freshwater species (topmough gude-

gon, Pseudorasbora parva (Britton and Brazier 2006;

Britton et al. 2010); fathead minnow, Pimephales

promelas; black bullhead, Ameiurus melas; African

clawed-frog, Xenopus leavis; American bullfrog,

Lithobates catesbeianus; and, water primrose, Luwi-

gia grandiflora (Defra 2015). An important difference

between our data and experience from GB to date is

that the NNRM scheme indicates terrestrial plants

2414 O. Booy et al.

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could be a high priority for eradication where limited

to small populations; however, there are few recorded

eradications of these species in GB, or indeed in

Europe (Genovesi 2005). We suggest this is because

terrestrial plants are often ‘sleeper weeds’ (Groves

1999) being overlooked at the early stages invasion,

with decisions to attempt management taken too late

for eradication to be feasible or cost effective. This

indicates that greater care should be taken in the future

to identify and eradicate potentially invasive terrestrial

plants at the earliest opportunity.

This work could be developed in a number of ways.

The focus of the scheme is on eradication; however,

further tools (or an extension of this scheme) to

prioritise species for prevention interventions and long

term management are required. Advances have been

made in this area in the field of pest and weed risk

management (e.g. Auld 2012; FAO 2011; Johnson

2009; Kehlenbeck et al. 2012; Setterfield et al. 2010;

Virtue 2010) and similar approaches may be applica-

ble to the broader field of INNS. To aid consistency

and repeatability it is important that assessors can

clearly define invasion scenarios, eradication strate-

gies and distinguish between the predefined responses

used in the semi-quantitative scoring scale. We

provide guidance for this purpose; however, further

elaborations of the scheme may benefit from refining

these further, in particular providing more prescriptive

instructions for defining invasion scenarios based on

population size and scale; using separate experts to

define the scenario than those undertaking the assess-

ment; testing the use of multiple scenarios and

eradication strategies for individual species; and,

further defining and calibrating the response and

confidence scales. A simple assessment of confidence

has been presented here, but novel methods have been

developed to better utilise and communicate uncer-

tainty that could further enhance the scheme (e.g. Holt

et al. 2012).

While applied here at a national level, the scheme is

designed for use at any scale from specific sites to

continent wide. Indeed, it may be timely to apply the

approach across the EU given the requirements for risk

management included in the recently adopted Regula-

tion for Invasive Alien Species (Genovesi et al. 2015).

Acknowledgements This work was funded, in part, by the

Animal and Plant Health Agency. HER receives support from

the Joint Nature Conservation Committee and the Natural

Environment Research Council (via National Capability

funding to the Centre for Ecology and Hydrology, Project

EC04932). We are grateful to Sonia Vanderhoeven, Johan

Naslund and Steve Rushton for comments on the manuscript, as

well as all of the experts, risk managers and policy officials that

helped throughout the development of the scheme.

Open Access This article is distributed under the terms of the

Creative Commons Attribution 4.0 International License (http://

creativecommons.org/licenses/by/4.0/), which permits unre-

stricted use, distribution, and reproduction in any medium,

provided you give appropriate credit to the original

author(s) and the source, provide a link to the Creative Com-

mons license, and indicate if changes were made.

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